Existing and emerging cyanocidal compounds: newperspectives for cyanobacterial bloom mitigation

Hans C. P. Matthijs . Daniel Jancula .

Petra M. Visser . Blahoslav Marsalek

Received: 31 March 2016 / Accepted: 5 April 2016! The Author(s) 2016. This article is published with open access at Springerlink.com

Abstract To help ban the use of general toxicalgicides, research efforts are now directed towards

the discovery of compounds that are specifically

acting as cyanocides. Here, we review the past andlook forward into the future, where the less desirable

general algicides like copper sulphate, diuron or

endothall may become replaced by compounds thatshow better specificity for cyanobacteria and are

biodegradable or transform into non-toxic products

after application. For a range of products, we reviewthe activity, the mode of action, effectiveness, dura-

bility, toxicity towards non-target species, plus costs

involved, and discuss the experience with andprospects for small water volume interventions up to

the mitigation of entire lakes; we arrive at recommen-dations for a series of natural products and extracted

organic compounds or derived synthetic homologues

with promising cyanocidal properties, and brieflymention emerging nanoparticle applications. Finally,

we detail on the recently introduced application of

hydrogen peroxide for the selective killing ofcyanobacteria in freshwater lakes.

Keywords Algicides ! Cyanocides ! Hydrogenperoxide ! Lake mitigation ! Sustainability

Introduction

Eutrophication and climate change cause massive

growth of cyanobacteria in water bodies across the

world (Johnk et al. 2008; Paerl and Huisman 2008).Several publications presented in this special issue of

Aquatic Ecology entitled ‘‘Cyanobacterial bloom.

Ecology, prevention, mitigation and control’’ reflectthis statement at large. Dense populations of

cyanobacteria that may float on the surface of lakes

are called water blooms and are regarded as asymptom of poor water quality. Nuisance is not only

esthetical, a decrease in species richness also threatensbiodiversity. Notably, cyanobacteria are most feared

because of their potential to produce health-affecting

toxins and odorous compounds that restrict the usageof lakes and of lake water for a range of ecosystem

Guest editors: Petra M. Visser, Bas W. Ibelings, Jutta Fastner& Myriam Bormans/Cyanobacterial blooms. Ecology,prevention, mitigation and control.

H. C. P. Matthijs ! P. M. Visser (&)Department of Aquatic Microbiology, Institute forBiodiversity and Ecosystem Dynamics, University ofAmsterdam, P.O. Box 94248, 1090 GE Amsterdam, TheNetherlandse-mail: p.m.visser@uva.nl

D. Jancula ! B. MarsalekInstitute of Botany, Academy of Sciences of the CzechRepublic, Lidicka 25/27, 602 00 Brno, Czech Republic

B. MarsalekRECETOX - Research Centre for Toxic Compounds inthe Environment, Masaryk University, Kamenice 5,625 00 Brno, Czech Republic

123

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DOI 10.1007/s10452-016-9577-0

services of considerable importance for societal andeconomic interests, including drinking water, irriga-

tion, aquaculture, fish breeding, and recreation.

Cyanobacterial problems are universal and have beenincreasing for the last four decades. Ideally, all

solutions should promote reversal of eutrophication

and limit nutrient inputs into the lake from itscatchment area and from diverse anthropogenic

sources. Supporting methods include irreversible

deposition of already-present phosphate in the lakebody on its sediment with polyvalent metal ions like

Al covalently attached to a mineral matrix (e.g.

Jancula and Marsalek 2011a; Lurling and Oosterhout2013). Though urgent and widely advocated, re-

oligotrophication solutions will also require restric-

tions on nutrient release in the catchment area (Cobo2015) next to considerable engineering investments

for nutrient reduction.

Independently or as a complementary effort to re-oligotrophication, application of algicides is seen as a

relatively fast and financially affordable control of the

growth of noxious phytoplankton species. Muchattention has been given in recent decades to strategies

for cyanobacterial bloom management that are based

on general algicidal approaches, while specificcyanocidal methods have become fashionable only

more recently.

We present an inventory of algicides in ‘‘Conven-tional chemicals in use as algicides’’ section, and in

‘‘Perspectives and prospects of preferred cyanocides’’

section, we survey compounds that are more specificfor cyanobacteria, and they are defined as cyanocides

in this review. The focus is on compounds and

methods that next to cyanocidal specificity demon-strate good prospects for sustainability in lake miti-

gation at reasonable costs. In this manuscript,

sustainability and sustainable mitigation are reservedfor methods of which usage facilitates lake systems to

retain a diverse and productive biological state

indefinitely.

Conventional chemicals in use as algicides

Conventional algicides comprise herbicides likediuron or endothall, and other algicidal compounds

with copper or potassium. All feature affordable

pricing, easy availability on the market, easy manip-ulation during applications, and last but not least all

exert the desired rapid inhibitory effects on the growthof phytoplankton. However, we will discuss that these

algicides demonstrate poor cyanocidal specificity and/

or fail to settle with the sustainability principle.

Herbicides

Herbicides are a group of pesticides for control of bothterrestrial and aquatic plants. Since their use is based

mainly on inhibition of photosynthesis, it was a

legitimate assumption that such chemicals can beused in control of green algae and also cyanobacteria

in lakes, reservoirs and aquaria without affecting non-

phototrophic life.Diuron (3-[3,4-dichlorophenyl]-1,1-dimethylurea)

acts as an inhibitor of photosynthesis and binds to the

quinone acceptor side of photosystem II in oxygenicphotoautotrophs and by that blocks light-driven elec-

tron transfer (Giacomazzi and Cochet 2004). Diuron is

applied in a wide concentration range from micro-grams to milligrams of herbicide per litre of water

(Zimba et al. 2002; Magnusson et al. 2010). Although

diuron is very effective in removal of nuisancephytoplankton, it has two disadvantages:

(a) persistence in sediments (up to 1 year) (Fieldet al. 2003; Okamura et al. 2003), and

(b) non-selectivity, i.e. it can harm also other biota

in aquatic ecosystems (Giacomazzi and Cochet2004). Moreover, diuron is subjected to degra-

dation in the environment, leading to formation

of 3,4-DCA (3,4-dichloraniline), which is ahighly toxic substance possessing genotoxic

properties (Osano et al. 2002).

Endothall (7-oxabicyclo[2.2.1]heptane-2,3-dicar-

boxylic acid) is known as a contact herbicide currentlyavailable in many modifications, and its mode of

action is through interference with RNA synthesis.

Endothall acts selectively against cyanobacteria, muchmore so than with green algae and fish, but the

relatively high toxicity towards aquatic invertebrates

is problematic (Holdren et al. 2001). Endothallrequires application at higher concentrations than

diuron to control cyanobacterial species. It was also

found that after long-term application, affected pop-ulations may build up resistance to this herbicide

(Prosecka et al. 2009).

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Several other herbicides that have been tested aspotential effective algicides include diquat, paraquat

(Schrader et al. 1998), atrazine and simazine (Peterson

et al. 1994). While these algicides are very effective asnon-specific cyanocides, a warning has been published

that the use of paraquat (at 1 mM final concentration)

resulted in a 90 % increase in detectable cyanotoxinsin the water (Ross et al. 2006). This potential

cyanotoxin release from dying cells of cyanobacteria

after treatment with algicides is a general problem (cf.‘‘Concluding remarks’’ section at the end of this

review). Otherwise, and generally speaking, the

a-specific toxicity of herbicides has already limitedapplications and should further restrict usage in

aquatic systems.

Algicidal function of copper

The application of copper-based compounds is one ofthe most frequently used methods to control phyto-

plankton abundancy. Preference for its use is based on

functional effectiveness, ease of application and lastbut not least low costs. Copper is applied in different

formulations, and next to copper sulphate, other forms

like copper oxychloride, organo-copper complexeslike copper ethanolamine complex (cutrine) or copper

citrate are used in commercial preparations (Murray-

Gulde et al. 2002; Zhao et al. 2009; Qian et al. 2010;Calomeni et al. 2014). Concentrations used are in the

range of hundreds of micrograms Cu L-1 (Jancula and

Marsalek 2011a; Fan et al. 2013). The principle ofalgicidal activity is through presence of bioavailable

Cu2? ion that can denature enzymes, affect membrane

permeability, and decrease photosynthetic activity,phosphorus uptake, and nitrogen fixation (Zhou et al.

2013). The toxicity is not very rapidly evident and may

require several days for completion, while the rate ofcopper disappearance to the sediment counteracts the

wanted algicidal function (Qian et al. 2010).

The toxicity of copper to aquatic biota in standardlaboratory conditions decreases in the order crustacean

(10 lg L-1), cyanobacteria (20 lg L-1), algae anddiatoms (20–100 lg L-1), rotatoria, snails, amphibians

and submersed macrophytes (100–400 lg L-1), up to

the less sensitive organisms like fishes (400 lg L-1–12 mg L-1) (Cooke et al. 2005; Zhao et al. 2009; Seder-

Colomina et al. 2013). These data and empirical

observations have suggested that copper is more toxicfor cyanobacteria than to other aquatic biota and that

copper compounds could serve as cyanocide. However,it must be considered that the bioavailability of copper

after application in aquatic ecosystems is modified by

pH, organic carbon, alkalinity, ionic strength, presenceof organic (e.g. humic) substances, or conductivity and

that the narrow concentration range between general

algicidal and the wanted more specific cyanocidalfunctionality likely limits the selective application of

copper as a specific cyanocide (Mastin and Rodgers

2000). It is also considered that the duration ofcyanostatical effects of copper in aquatic ecosystems

lasts for around 1 week only, which is due to rapid loss

from the water phase through precipitation of copper asinsoluble salts and hydroxylates (Cooke et al. 1993;

Zhou et al. 2013; Fan et al. 2013). A need for longer-

term effectiveness requires repeated treatments, creat-ing the problem of accumulation of Cu in the sediment

with unknown risks for potential harm to diverse benthic

life (Jancula andMarsalek 2011b). Additionally, chron-ical application may induce resistance and cause shifts

in the composition of the phytoplankton community

with prevalence of copper-resistant green algae (Qianet al. 2010; Rouco et al. 2014). The ecotoxicological

properties of any algicidal agent must be taken into

account prior to actual in situ ecosystem application.Next to persistence of copper another issue in treatment

of harmful cyanobacterial blooms is the release of

cyanotoxins like microcystin-LR (MC-LR) by Micro-cystis aeruginosa (Jones and Orr 1994). Because this is

true for all algicidal or cyanocidal compounds, the topic

is discussed in some more detail in the generalconclusions. The side effects of copper are seen as less

desirable, and its use in ecosystems is disputable in view

of sustainability principles. Despite these considera-tions, copper is still one of the most used algicides.

Potassium chloride

The addition of low amounts of potassium ions (K?) has

been suggested as a method to selectively combatharmful cyanobacterial blooms (Parker et al. 1997;

Kolmakov 2006; Shukla and Rai 2007).M. aeruginosastrain PCC 7806 appears to be more sensitive to low

concentrations of potassium ions (1–5 mmol L-1) than

to other alkalimetal cations such as sodium (Parker et al.1997). However, a recent survey of potassium ion

sensitivity in a variety of Microcystis strains showed

quite distinctive differences (Sandrini et al. 2015).Based on these results, the general cyanocidal

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effectiveness of potassium-ion is less evident and risksof less sensitive successors to take over in the ecosystem

disfavour application of this cyanocide.

Perspectives and prospects of preferred cyanocides

More recently introduced algicides and cyanocides

comprise chemicals and natural products that have

promising potential to replace the currently used lessdesirable compounds discussed in ‘‘Conventional chem-

icals in use as algicides’’ section. At present, the prices of

many natural products described below are usuallyhigher than for conventional products, but in prospect the

potential advantages comprise at least two desirable

properties: (1) selective toxicity towards only cyanobac-teria in the phytoplankton, and minimized toxicity

towards non-phototropic biota and (2) biological degra-

dation, for optimal sustainability. In ‘‘Perspectives andprospects of preferred cyanocides’’ section, we describe

three main areas for development of such products and

applications. ‘‘Natural compounds’’ section focuses onthe use of natural compounds prior to purification and

separation, ‘‘Isolated natural compounds, including

synthetic homologues’’ section deals with more definedchemical compounds derived from the natural starting

materials discussed in ‘‘Natural compounds’’ section , in

‘‘Nanomaterials’’ section, emerging prospects of nan-otechnology are discussed, and ‘‘Hydrogen peroxide’’

section focuses on the use of hydrogen peroxide and

briefly makes mention of other oxidative approaches tosuppress phytoplankton.

Natural compounds

Search for effective compounds will always raise an

interest in cheap and easily available natural products.Nowadays hundreds of isolated compounds or extracts

thereof have been tested towards harmful phytoplank-

ton species. Here, we review products which couldone day replace conventional chemicals in the battle

against cyanobacterial blooms. Most of the productsdiscussedwere tested not only in the laboratory but also

in natural conditions.

Barley straw

The best known and most studied natural product usedagainst both green algae and cyanobacteria is barley

straw despite opposing results in applications and lackof convincing background information on the mecha-

nism of action (Iredale et al. 2012). The first report

about the use of barley straw as a technique to suppressthe growth of harmful phytoplankton was in the 80s

(Welch et al. 1990; Newman and Barrett 1993; Barrett

et al. 1999; Brownlee et al. 2003). The first study wasnot specifically against cyanobacteria, but against the

green alga Cladophora glomerata in the Chesterfield

canal (Welch et al. 1990). Whereas no effect on algaewas observed during the first season after the introduc-

tion of straw, algae abundance decreased in the three

subsequent years by 90 %. One of the first in situapplications took place at the Derbyshire reservoir in

1994 (Everall and Lees 1996). Addition of 50 g m-3 of

barley straw appeared to control cyanobacterial growthand was stated to be due to production of unspecified

phytotoxins. Moreover, the authors observed no evi-

dence of environmental impact on other biota, and evenan enhanced invertebrate productivity was noticed.

However, barley straw acts in a general algistatic way

and prevents growth of all phytoplankton rather thanbeing specific against cyanobacteria. Barley straw has

been added as large bales inwater canals, and asminced

straw or as a liquid barley extract in entire water bodies,and has in several cases shown positive effects on water

quality. The combination of its relatively low price,

natural origin, and general availability (also includingrice straw, discussed in ‘‘Rice straw’’ section) has

justified its choice. The method cannot yet be recom-

mended for general applications, because (1) barleystraw does not affect harmful phytoplankton immedi-

ately (which has led to quite some speculations about

the mode of action which is not yet sufficientlyclarified); (2) introduction of oxygen demand needed

for the degradation of the biomass added to the water is

a less desirable side effect that could be overcome byuse of extracts; and (3) until now only few field studies

have been undertaken and have presented contradictory

results (Huallachain and Fenton 2010; Spencer andLembi 2007). As an example of an unsuccessful

application, we may mention a study by Prygiel et al.(2014) describing the attempt to improve the water

quality at the Pont-Rouge reservoir in Northern France.

Three tons of barley straw bales were introduced intothe water to reach the recommended value of 50 g of

straw per m3. Unfortunately, although the addition was

performed before the summer (beginning of May), itdid not prevent the formation of cyanobacterial blooms,

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though it must be remembered that it may still proveeffective later in time (Welch et al. 1990).

For the mode of action of barley straw many

hypotheses have been suggested. One of the firsttheories was the generation of hydrogen peroxide

during the photooxidation of a particular constituent in

the straw (Everall and Lees 1997). Iredale et al. (2012)determined that many different variables may deter-

mine the cyanocidal effects of barley straw, for

example the actual cyanobacterium strains involved,the amount of UV-supplemented visible light, the

temperature, the physical state of the straw used, i.e.

minced or as bales, with minced material workingfaster, the state of decomposition of the straw, etc.

They also provide clear evidence that formation of

hydrogen peroxide during the photooxidation of ligninand quinone from degrading straw may exert effective

cyanocidal activity. The actual cyanocidal specificity

of hydrogen peroxide has in the meantime beenconsolidated and is discussed in the ‘‘Hydrogen

peroxide’’ section of this review. Additionally, ellagic

acid isolated from straw demonstrated significantcyanocidal effects against M. aeruginosa (Macioszek

et al. 2010). A range of phenolic and quinone

compounds extracted from barley straw has beenstudied. Thirty-eight compounds (earlier identified as

products of barley straw decomposition) were tested

(Murray et al. 2010). Results revealed highly effectivecyanocidal toxicity of 2-phenylphenol, benzaldehyde,

3-methylbutanoic acid, and p-Cresol. The latest

investigations showed that a pair of chiral flavonolig-nans called salcolin A and B demonstrated EC50’s

(concentration for 50 % of maximal effect) of

6.02 9 10-5 and 9.60 9 10-5 mol L-1, respectively,against Microcystis sp. (Xiao et al. 2014). Hence, this

range of compounds could very well contribute to the

cyanocidal properties of barley straw.

Rice straw

Rice serves as an important food source for human

being across the world, and this suggested the use ofrice straw as an algicide and cyanocide very much like

barley straw. Rice hull is the major by-product of

milling and represents approximately 20 % of therough grain weight (Xuan et al. 2003). Rice hulls are

plentiful at hand and were tested as an environmen-

tally friendly and sustainable source for algicideproduction (Park et al. 2009). Unfortunately, the less

abundant rice straw appeared to be more effective andselective towards cyanobacteria than hulls (Jia et al.

2014).

The first study describing the effects of rice strawon the growth of cyanobacteria was published even

earlier than for barley straw (Rice et al. 1980). Lately,

renewed attention was paid to this fundamental workand it was discovered that even a concentration of rice

straw extract of as little as 0.01 mg L-1 inhibits the

growth of M. aeruginosa (Park et al. 2006). In thesame study, the authors also identified several chem-

icals which could be responsible for the inhibitory

effects of rice straw on cyanobacteria. Salicylic acidwas proposed although the highest inhibitory effi-

ciency was only 26 %. The authors suggested that

salicylic acid may act together with other (mainlyphenolic) compounds found in extracts in a synergistic

way. Later on, other compounds as b-sitosterol-b-D-glucoside and dicyclohexanyl orizane which power-fully inhibited growth ofM. aeruginosa (66 and 80 %

growth inhibition for b-sitosterol-b-D-glucoside and

dicyclohexanyl orizane, respectively) at concentra-tions of 100 lg L-1 of the particular compound, were

purified. Other active compounds from rice have been

isolated, but the cyanocidal efficiency of these com-pounds was much lower (Ahmad et al. 2013).

To date, only one study assessed the use of rice straw

against a natural assemblage of cyanobacteria (Jia et al.2014). For this study, enclosures were used

(6 m 9 5 m 9 2.2 m) in the shallow Lake Taihu

(China) to test rice straw (1 g L-1) and the efficiencyin combination with hydrogen peroxide (10 mg L-1). In

this combination, hydrogenperoxidewas supposed to act

as a rapid cyanocide, and rice straw was anticipated as alonger-term measure to remain active during overwin-

tering and at the moment of recruitment of Microcystis

from the sediment in spring. As a result, the biomass ofcyanobacteria decreased by 27.1 % during recruitment

and by 53.2 % of the first algal bloom compared to the

year before (Jia et al. 2014).Unfortunately, the efficiencyof rice straw by itself remains unknown.

Isolated natural compounds, including synthetic

homologues

Ephedra equisetina root extracts

Use of purified plant extracts to control harmful algaein natural water bodies seems unrealistic because of

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limited plant material availability facing the volumet-ric demands of natural water bodies, yet pioneering

attempts were launched by Yan et al. (2012). Authors

applied root extracts into six ponds in China in a finalconcentration of 87.5 ll L-1 (equivalent to

1.25 mg L-1 of dried Ephedra equisetina root). The

application was successful in terms of a significantdecrease in cyanobacteria (expressed as chlorophyll-

a concentration). TheM. aeruginosa population in the

treated ponds was reduced to values of 95–300 lg L-1

Chl-a, whereas the concentration in control ponds was

found to be 510–680 lg L-1 Chl-a (average decrease

of 67 %). Moreover, it was shown that fish survivalrates and fish yields in the control and treated ponds

were not significantly different. In applications using

extracts, the authors monitored zooplankton andmacrophytes and concluded that no negative impacts

on the pond ecosystems were observed and that habitat

conditions for macrophytes, zooplankton, and bacte-rioplankton numbers even improved.

Interestingly, the extract was discovered to be more

cyanocidal (causing cell death) than cyanostatical(causing inhibition of cell proliferation). Results from

both in situ and in vitro trials showed destruction of the

thylakoid membranes, interruption of electron trans-port, reduction in effective quantum yield, and

cyanobacterial death (Yan et al. 2012). To this date,

unfortunately, application of E. equisetina extracts hasbeen repeated neither in situ nor in in vitro experi-

ments, and thus, this study remains for now the only

evidence of the great potential that this plant speciesproduct may have in the mitigation of cyanobacteria.

Given availability of the product, applications may be

especially well suited for fountains, or ornamentalponds with a low water volume.

It is recommended that research contributing to the

identification and isolation of cyanocidal active com-pounds from plant materials will be continued. The

undesirable accumulation of organicmaterial in lakes as

a negative side effect of the use of raw natural productsas suchcan be limited in thatway. In particular, attention

should be paid to the selection of the raw resource forproduction which ideally should avoid the need for

competitive use of precious crop land.

Anthraquinones

Perhaps the best known is 9,10-anthraquinone which isable to inhibit the growth of musty odour-producing

cyanobacterium Oscillatoria perornata at concentra-tions of around 1 lM under laboratory conditions

(Schrader et al. 1998). Investigation of the mode of

action resulted in the statement that 9,10-anthraquinoneinhibits photosynthetic electron transport, probably at

PSII, and thereby affects growth (Schrader et al. 2000).

It also causes thylakoid disorganization (identical to thereported modification in a cyanobacterium treated with

simazine) and reduces the number of ribosomes

(Schrader et al. 2000). Unfortunately, this compounddid not effectively reduce the abundance of cyanobac-

teria in catfish production ponds, possibly due to its

early precipitation (Schrader et al. 2003). To providebetter solubility, 9,10-anthraquinone was modified to

anthraquinone-59 (2-[methylamino-N-(1-methy-

lethyl)]-9,10-anthraquinone). By use of micro-titreplate bioassays, this novel compound was found to be

much more selectively toxic towards O. perornata than

diuron and copper sulphate, and in studies using limnocorrals placed in catfish production ponds for gradual

release, application rates of 0.3 lM (125 lg L-1) of

the anthraquinone-59 drastically reduced the abun-dance of O. perornata and levels of 2-methylisobor-

neol, the musty compound produced by O. perornata

(Schrader et al. 2003). More water-soluble anthraqui-none analogues with interesting ecotoxicological prop-

erties have been synthesized recently (Nanayakkara

and Schrader 2008).

L-Lysine

A first report on lysine indicated that both D- and L-

lysine were potent inhibitors ofMicrocystis sp. growth

(Kaya and Sano 1996). Five years later, the L-isoformwas established to be effective and the D-isoform was

reported as ineffective (Zimba et al. 2001). According

to Zimba et al. (2001), L-lysine was effective alsoagainst other cyanobacterial species such as Pseudan-

abaena articulata and Planktothrix perornata but less

effective towards the green alga Scenedesmus dimor-phus (Chlorophyta). Similar results were confirmed by

Hehmann et al. (2002) who observed a markedinhibitory impact of L-lysine against Microcystis spp.

In contrast, other cyanobacteria (Oscillatoria rubes-

cens, Phormidium tenue) as well as Bacillariophyceaespecies (Melosira granulata, Cyclotella meneghini-

ana) and green algae (Scenedesmus acutus, Pedias-

trum duplex) showed much less impairment of growthafter lysine addition (Hehmann et al. 2002).

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Experiments conducted in outdoor ponds nextconfirmed the laboratory tests. To ponds with a water

volume of 20 m3 and natural Microcystis blooms,

7.3 mg L-1 (final concentration of L-lysin) was addedand also applied on the water surface to affect floating

cyanobacteria directly (Takamura et al. 2004). The

Microcystis removal was rapid, already after 2 daysMicrocystis colonies vanished from the water surface.

After the disappearance of Microcystis, Euglena sp.

and/or Phormidium tenue emerged and became thedominant species in the phytoplankton community of

the pond. Though the effective duration of the

reduction in cyanobacteria has been indicated as shortterm (Lurling and Oosterhout 2014), further interro-

gation of this interesting cyanocide is recommended

and should include sustainability aspects (increase inorganic matter, cyanotoxin release), and questions

about cyanobacterial strain succession as suggested by

the discrepancies in strain sensitivity for L-lysine.

Sanguinarine

The effects of aqueous root extracts from species of the

family Papaveraceae on the growth of cyanobacteria,

algae, and non-target aquatic organisms were investi-gated by Jancula et al. (2007). The EC50 forMicrocystis

sp. was found to be 57.11 and 55.81 mg L-1 of root dry

weight from Chelidonium majus and Dicranostigmalactucoides. Assessment of the ecotoxicological prop-

erties of isolated sanguinarine suggested that the

toxicity of these root extracts (Jancula et al. 2009)was probably caused by this alkaloid. The results were

confirmed by Yi et al. (2013) who isolated and tested

sanguinarine fromMacleaya microcarpa. Sanguinarinewas active againstM. aeruginosawith a 3 d-EC50 value

of 0.47 and a 7 d-EC50 value of 0.36 mg L-1. In

contrast, sanguinarine showed low inhibition forChlorella pyrenoidosa and Scenedesmus obliquus with

3 d-EC50 value of 5.37 mg L-1 (Yi et al. 2013). Even

better results were achieved by Shao et al. (2013) whodetermined a cyanocidal EC50 of 34.5 lg L-1 for M.

aeruginosa strain NIES-843, and search for the poten-tial mode of action highlighted both the donor and

acceptor site of the photosystem II reaction centre to act

as likely targets for inhibition by sanguinarine. In anextended analysis, damage to DNA and production of

oxidative stress in actively growing cells emerged as

noticeable additional effects of sanguinarine.

Nanomaterials

Nanomaterials are nowadays used in many areas ofindustry, medicine or in everyday life. Growing

concern about a multitude of (plastic) nanomaterials

to be a threat for natural ecosystems via their intensiveinteraction with living organisms is mentioned, but

does not apply to nanoparticles of zerovalent iron

(nZVI) of which the initial and functional cyanocidaleffect is cell lysis and thereafter the primarily effective

nZVI product is readily transformed in non-toxic

aggregated Fe(OH)3, which promotes flocculation ofthe cell debris, binds residual phosphate compounds

and promotes gradual settling of the cyanobacterial

biomass on the sediment (Marsalek et al. 2012). Thepotential of the nZVI method for cyanobacterial

bloom control still awaits further study, including

survey of longer-term and chronic application effects.Next to iron, also silver nanoparticles have been

tested against cyanobacterial blooms. Although large-

scale application of nanosilver into aquatic ecosys-tems is hard to imagine, Park et al. (2010) tested the

efficiency of nano-Ag towards M. aeruginosa. The

study shows that 1 mg L-1 of nano-Ag inhibited thegrowth of the toxic cyanobacteriumM. aeruginosa by

87 %, and similar results were obtained in field

experiments. Moreover, M. aeruginosa proved to bemore sensitive to silver nanoparticles than green algae

were.

Nanosilicate pellets (derived from natural clayminerals) (NSP) have been suggested to act against

cyanobacterial blooms and cyanobacterial toxins by

Chang et al. (2014). The authors propose to use thenanosilicate material in both natural waters as well as

in drinking water treatment processes. Authors stress

that M. aeruginosa was more sensitive than othertested organisms (in particular if compared to other

bacteria), but data on how more diverse aquatic

species (green algae, invertebrates or fish) are affectedhave not been revealed till present.

Hydrogen peroxide

Natural prevalence of hydrogen peroxide (HP) in

water exposed to sunlight was shown to originate fromphotochemical conversion of organic constituents

such as humic substances (Cooper and Zika 1983),

as well as from physiologically mediated synthesis(Foyer and Noctor 2008). In defence against toxic

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reactive oxygen species (ROS), green algae possess awide repertoire of superoxide and peroxide neutraliz-

ing enzymes and the complementary reducing sub-

strates. Examples include the co-substrate-dependentenzymes ascorbate oxidase and thioreductase, next to

the reducing co-substrate-independent superoxide

dismutase and catalase enzymes (Dietz 2011; Schmittet al. 2014). The possible algicidal and cyanocidal and/

or cyanostatical activity of HP as formed during decay

of barley and rice straw have been mentioned alreadyin ‘‘Barley straw’’ and ‘‘Rice straw’’ sections of this

review. The rapid degradation of HP into just water

and oxygen is regarded as a great advantage in terms ofsustainability in comparison with many other cyanoci-

dal or cyanostatic substances described in earlier parts

of this review. While the latter may leave permanentresidues in the water or its sediment, the application of

HP leaves no traces of the added chemical. A

disadvantage is that handling of HP in concentratedform ([10 % w/v) requires qualified personnel. Based

on experience with present application technology

(Matthijs et al. 2012), upgrading of mitigation to lakeslarger than the current horizon of about 100 hectares

(250 acres) is realistic.

Mode of action of hydrogen peroxide

Early pioneering research with just HP demonstratedthat additions of as little as 1.75 mg L-1 of HP already

strongly inhibited photosynthesis and growth of the

cyanobacterium Oscillatoria rubescens (Barroin andFeuillade 1986). A sound explanation for the much

lower sensitivity of green algae to peroxide followed

from the discovery of a difference in the reactionmechanism during out-of-equilibrium-states of the

photosynthetic light and dark reactions. In short, if

chloroplasts (in green algae or isolated from plants)are exposed to high light or low Ci, molecular oxygen

serves as an alternative photosystem I electron accep-

tor replacing the insufficiently regenerated NADP?. Inchloroplasts of green algae, this escape route is known

as the Mehler reaction (Mehler 1951). The reductionof oxygen leads to the formation of superoxide anion,

which is enzymatically transformed by the enzyme

superoxide dismutase into HP, the latter is subse-quently degraded into just water and oxygen by

catalase or peroxidase enzymes (Asada 1999; Vassi-

lakaki and Pflugmacher 2008).

This reaction scheme is well known in plants, butquite surprisingly the similar Mehler reaction is not

present in cyanobacteria and is replaced by a Mehler-

like reaction which involves two flavodiiron proteinsthat produce water directly (Helman et al. 2003, 2005).

By consequence, no intermediary ROS compounds are

formed in cyanobacteria (Allahverdiyeva et al. 2013,2015). With no ROS compounds formed, the hypoth-

esis was put up that for cyanobacteria the need to

handle the ROS compounds superoxide and HP is lesscompulsory than in green algae, and hence that

cyanobacteria are likely more sensitive to HP than

eukaryotic algae. This fundamental idea suggested themechanism why HP could act as a specific cyanocide

which has earlier been demonstrated empirically

(Barroin and Feuillade 1986). This hypothesis wasthereafter successfully tested in the laboratory (Drab-

kova et al. 2007a, b; Weenink et al. 2015) and in the

field (Matthijs et al. 2012). The actual cyanobacteriakilling compound may very well be not HP itself but a

compound derived from HP, for which hydroxyl

radical formation by UV light and catalysed by Fentonreaction active ions has been presented as a candidate

by Huo et al. (2015).

HP has been empirically tested as a cyanocide and/orgeneral algicide by a range of authors, and widely

deviating dose–response observations for effectiveness

of HP versus cyanobacteria in lakes range from asmuchas 100 mg L-1 (Barrington and Ghadouani 2008;

Barrington et al. 2011, 2013) to around 60 mg L-1

(Wang et al. 2012; Gao et al. 2015), 10 mg L-1 (Jiaet al. 2014), to \5 mg L-1 (Barroin and Feuillade

1986; Drabkova et al. 2007b; Matthijs et al. 2012).

However, it is obvious that the higher the concentrationof HP applied, the higher the killing efficiency of

cyanobacteria will be, and conversely it must be argued

that in lake treatments the dose should be as low aspossible to avoid killing of non-target species and to

respect the principle of sustainability. In the Nether-

lands, dosing is for that reason restricted to a maximumof 5 mg L-1. Till present more than ten cyanobacteria

plaguedDutch lakeswere treated successfully (Matthijset al. 2012, unpublished results). Lakes had a wide

variety of species diversity, in which the predetermined

effective dose needed to be varied from a minimum of2.3 mg L-1 in most of the Planktothrix agardhii

dominated lakes to the maximally lawful upper limit

of 5 mg L-1 in some of the Microcystis dominatedlakes. Also, lakes dominated by nitrogen fixing

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cyanobacterial species Aphanizomenon and Dolichos-permum (formerly called Anabaena) have by now been

successfully treated with the cyanocide HP applied at

3–4 mg L -1 (unpublished results). Both strain typeand cell density are expected to contribute to the

differences in the required dose. It is therefore recom-

mended to estimate the minimal effective concentrationthe day before a treatment. In doing so, it is important to

state that up to 40 % of the pre-tested lake systems were

regarded as not suitable for treatment because acounteracting high rate of HP degradation versus a

low loss of photosynthetic vitality in the targeted

cyanobacteria was beyond an empirically determinedrange. This range is formulated as follows: a minimum

of 2 mg L-1 of peroxidemust be retained until 5 h after

the application of a maximal starting concentration of5 mg L-1. A successful treatment characteristically

demonstrates a loss of at least 80 % of photosynthetic

vitality (measured as photosynthetic yield loss in PAMfluorimetry of all phytoplankton) in 3–5 h after the

peroxide application, and near to a 100 % for the

subgroup of cyanobacteria. In the explanation of whysome lakes were considered not adequate for treatment,

we mention that the cell density of the phytoplankton,

and the phytoplankton species composition in the waterplays an important role. In particular, the presence of

eukaryotic algae (green algae and diatoms, with both

algal species bearing strong anti-ROS capacity) givesrise to a high rate of HP degradation, which effectively

protects cyanobacteria in the phytoplankton against

oxidative damage (Weenink et al. 2015; Weenink et al.unpublished results). Also colony morphology and EPS

richness play a pronounced role in resistance of

cyanobacteria to an attack by HP (Lurling et al. 2014;Gao et al. 2015). Interestingly, with green algae and

diatoms able to repair any relapse of their vitality within

24 h, renewed proliferation of cyanobacteria in thewater body does not take place for over 6 weeks or

possibly may only occur over the course of the next

growth season (Spencer and Lembi 2007;Matthijs et al.2012; Weenink et al. 2015, unpublished results).

Considerations about HP application

As earlier evidenced for other algicides, Lurling et al.(2014) warned for lack of degradation of microcystins

(MC) solubilized from HP-treated lysing cells of a

laboratory strain of Microcystis. However in fieldexperiments with the natural complement of

heterotrophic microorganisms present, the total ofextractable MC, i.e. the sum of particulate and water

soluble fractions, rapidly decreased by more than

90 % in \3 days (Matthijs et al. 2012). The latterobservations on rapid MC degradation are supported

by reports on microbial degradation of MC (Lawton

et al. 2011; Dziga et al. 2013) and hydroxyl radicalcatalysed processing of microcystin (Huo et al. 2015).

Dissolved organic compounds from decomposing

cell debris could result in higher biological andchemical oxygen demand with a risk for anaerobiosis

and fish kills, which could be argued to play a less

favourable role in anti-cyanocidal treatments includ-ing HP. In lake treatments with HP, this has been

inspected and judged as a lesser problem than

anticipated. Like the observations in the applicationof the cyanocide lysine by Takamura et al. (2004),

debris of dead cells sank rapidly from the water

surface in the water column and onwards to thesediment with clear water emerging in\48 h after the

treatment (unpublished results Weenink et al.). Fur-

thermore, while HP application is advised against incase the rate of HP degradation is too high, this

naturally limits the applicability in lake mitigation of

denser blooms. Increasing evidence that the control ofcyanobacteria after one HP application extends to the

remainder of the entire season (but not into the next

year as different from some of the observations withbarley straw, see ‘‘Barley straw’’ section) should

convince water managers to act timely, i.e. before the

bloom becomes too dense.It is concluded that given permissible general

phytoplankton composition and cyanobacterial bloom

density, homogeneously added low concentrations ofHP have promising potential to act as specific

cyanocide for a range of commonly encountered

harmful cyanobacterial strains in freshwater lakes.Positive properties are (1) HP acts very fast, and a lake

is safe for swimming (or other interrupted function-

ality) again after 3 days only; (2) good sustainability,no lasting chemical traces of the added HP, nor toxic

substances including released cyanotoxins or particu-late organic matter from dead cyanobacteria are

retained in the water body (note: this statement is

based on current knowledge from lake studies in theNetherlands; however, it may not hold true for each

and every case, appropriate controls on toxin release

and persistence should always be part of any treatmentprogramme); (3) damage to other phyto- and

Aquat Ecol

123

zooplankton species is none or limited, and HP at therecommended maximal cyanocidal concentration of

5 mg L-1 is also safe for macrofauna, fishes and

aquatic plants; (4) affordable costs. A range ofquestions has been formulated that still need to be

answered, including effects of HP on other prokary-

otes in the lake ecosystem and potential adverseeffects on nutrient cycles, as well as possibilities that

some cyanobacterial strains may prove resistant after

all and will conquer the lake ecosystem (Dziallas andGrossart 2011; Zilliges et al. 2011). Most of all, it is

stressed that for now the HP-based peroxide method

for lake mitigation establishes a tool for suppression ofcyanobacteria. Whether it can also be used to

contribute sustainably to lake water restoration by

providing conditions that help increase biodiversity(Weenink et al. 2015) and that will accelerate re-

oligotrophication is topic of current research at the

University of Amsterdam.

Other oxidative compounds with algicidal properties

Firstly, calcium peroxide CaP (tradename Solvay CAS

No. 1350-79-9) is a solid chemical that is often used as

an oxygen-liberating additive in sediment sanitation.At lower pH, typically around 6.5, part of the oxygen

liberation is replaced by HP production. However,

while HP is liberated Ca(OH)2 is produced, whichincreases the pH up to 11 and makes the partial HP

liberation change completely to oxygen production.

The intended function for the liberated oxygen is tosupply bacteria that are used for degradation of

xenobiotic compounds.

As a spin-off, use of slow release formulations ofCaP has been suggested for killing of cyanobacteria

locally on the sediment (Noyma et al. 2015). These

applications require control of CaP distribution,control of the rate of HP liberation, in combination

with the control of the pH. These requirements predict

that usage of CaP needs further investigation beforeapplication is realistic. Promising primary tests have

already been published (Cho and Lee 2002).Restraints to the admissible phytoplankton density

for selective effects of HP as a cyanocide, and the

reality of often encountered high bloom density duringthe growth season have invited treatments with

compounds with strong oxidative power, including

usage of higher concentrations of HP. These strongoxidant treatments do not easily qualify for lake

ecosystems, but may find application in waste waterprocessing. Fan et al. (2013) evaluated the effective-

ness of chlorine, HP, ozone and potassium perman-

ganate (KMnO4) using SYTOX green stainpermeation as a measure for changes in cell membrane

permeability. All of these oxidizing compounds

impair the cell membrane, and destroy cell integritywith arrest of growth of M. aeruginosa in dense

blooms. Chlorine (3 mg L-1) showed the strongest

ability to impair cell viability with cell lysis ratesranging from 0.640 to 3.82 h-1. Ozone at a dose of

6 mg L-1 induced 90 % of the cyanobacterial cells to

become permeable in 5 min only, and the cell lysisrate in presence of KMnO4 (at a final concentration of

10 mg L-1) was 0.829 h-1. Though the oxidative

power of HP is not much different, it proved theweakest permeation agent, when added at a concen-

tration 10 mg L-1 it was shown to render no more

than 50 % of the cells to become permeable after1 day and about 85 % of permeable cells after 2 days,

after which increase in permeation changed to a

reversal, with regain of cell integrity (and growth)starting at day 3 and complete recovery reached at day

7. These data agree with the observations discussed in

the HP section above, where it is shown that HPeffectiveness relies on the initial reaction rate; if HP

action is as slow as in the Fan et al. (2013) study,

reversal is indeed expected, though a mechanisticexplanation and definition of the point of no return

value in HP application remains to be proposed.

Conclusions and discussion

Table 1 presents a summary of compounds discussed

in this review, showing their mode of action, and

effectiveness as specific cyanocide, their ecosafetyand related sustainability, the applicable dose range,

the market price per metric ton (1000 kg), with some

specific comments added. Note that only few of thelisted compounds in Table 1 are actually indicated to

be specific cyanocides, and in particular those com-pounds optimally fit the purpose of our survey and

highlight new perspectives for selective and sustain-

able cyanobacterial bloom mitigation. However, nextto apparent effectiveness additional aspects have to be

considered before compounds can be declared suit-

able for sustainable application. For example,endothall renders mutants, which strongly depreciates

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Table 1 An overview of several algicidal and/or cyanocidalcompounds with a description of their mode of action, theireffectiveness as cyanocide, algicide and their ecosafety and

related sustainability, the applicable dose range, and theestimated market price per metric ton (1000 kg)

Method name Effect Effectiveness Dose perlitre

Price per ton Comments

Mode of action Specificcyanocide

Generalalgicide

Ecosafety

Diuron Electrontransferblocking nearPSII

- ? - lg–mga $1–100 Toxicd degradationproducts

Endothall Proteinphosphataseinhibitor

? - - mgb $1–100 Renders mutants

Diquat PSI electrontransferinterferenceinhibition

- ? - lg–mga $1–100 Toxic, persistent

Paraquat PSI electrontransferinterferenceinhibition

- ? - lg–mga $1–100 Toxic, persistent

Atrazine Electrontransferblocking nearPSII

- ? ± lg–mga $2–16 Toxic, persistent

Simazine Flow ofelectrons toPSI inhibitor

- ? - lg–mga $2–200 Toxic, persistent

Copper Substitution ofMg2? inenzyme andcofactors

- ? - lg–mga $2–5 Heavy metal, lack ofspecificity

Iron Algalprecipitationin water

- ? ? mgb $100–200 Redox labile

Aluminm Algalprecipitationin water

- ? ± mga $100–200 Prevention of free Al(III)ion formation care foralkaline pH

Potassium Ion balancedisequilibrium

? - - mga $100–200 Impact on populationdynamics

Barley straw Not clarified yet - ? ? mg–gc $80–100 Non-predictable efficacy,raises BOD increase

Rice straw Not clarified yet - - ? mg–gc $100–150 No proven efficacy, raisesBOD

Ephedra rootextract

Not clarified yet ? ? ? lg–mg $30,000–40,000 Special small-volumepurpose only, naturalresource

Anthraquinones PSII electrontransportinhibition

? ? ? lg–mgb $3,000,000 Special small-volumepurpose only; price fornatural resource;synthetic compound ischeaper

L-Lysine Cell lysis ± - ? mgc $1000–2000 Limited strain sensitivityand effectiveness

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its use for obvious reasons of ecosafety. Potassiumsalts have been applied as specific cyanocides, but

may in a dose-dependent way give rise to shifts of

strains and species in an existing cyanobacterialcommunity, and thus may risk exchange for more

toxic species. For compounds like Ephedra root

extract, natural anthraquinones and sanguinarine priceconsiderations may apply and be seen as out-of-scope

pricewise, yet for small-volume applications these

compounds may perfectly well suit the needs, andavailable synthetic homologues may be considered. L-

lysine effectiveness as a cyanocide has been reported

forMicrocystis, but its efficacy for other strains is lessevident and growth inhibition lasts for a limited time

only. HP has a proven record of specific effectiveness

as a cyanocide, as cheap, but in concentrated formhandling and the essential issue of homogeneous

dosing of this reactive chemical in a water body needs

cost-raising qualified personnel.Several compounds listed in Table 1 have a wider

range of general algicidal effectiveness. Some have

the additional disadvantages of being toxic for otherforms of life and being persistent in the environment.

Their application will suppress not only the targeted

cyanobacteria, but at the same time will kill otherphytoplankton species with an important role in the

biological food chain (green algae, diatoms).

Other general algicides in Table 1 have a workingmechanism that may be classified as mostly primary or

secondary. Primary mechanisms are those that inter-

fere with phytoplankton by promoting mechanicallyforced cell lysis and resulting in direct coagulation and

precipitation. To this category belong zero valency

(elemental) iron particles that according to thesuggested definition appear adequate as algicides.

The used iron nanoparticles act only shortly as cell

lysing nanoparticles and next condense to much largeriron(III) hydroxide flocks that retain activity in the

deposition of biomass, a function also attributed to Al

polyhydroxylate and zeolites. The current price fornZVI is not really promoting its actual application.

Secondary mechanism examples provide rather

Table 1 continued

Method name Effect Effectiveness Dose perlitre

Price per ton Comments

Mode of action Specificcyanocide

Generalalgicide

Ecosafety

Sanguinarine PSII inhibition ? ? ? lg $10,000–40,000 Small-volume applicationonly

nZVI Membraneleaks,aggregation,precipitation

? ? ? mgb $35,000–150,000 Fe nano particles, potentialmembrane damage toother biota?

Hydrogenperoxide

Cyanobacterialack sufficientanti ROScapacity:selective celldeath

? ?e ? 1–5 (upto[100)mgc

$500–2000f In high concentration stockcorrosive, handling byspecialists only

Ozone,chlorine,permanganate

General strongOxidativedamage rapidmembranepermeation

- ? - 1–10 mg $200–500g Non-selective, algicides,highly effective, complexapplication, used fordrinking water and wastewater sanitation

3 mg n.a.

10 mg n.a.

a–c Educated estimate of the most probable treatment frequency: alikely\ one time yearly with occasional maintenance; bone time,but needs continuous additional care; c needs possibly to be repeated each year and may be even within a single growth seasond Toxic refers to effects on zooplankton invertebrates and young fishe At higher dosef Includes costs for on site delivery, price differs per truck load or smaller volumesg Ozone generator electrical power costs for on site production

Aquat Ecol

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cyanostatical effectiveness and include binding ofphosphate by mineral–metal compounds that facilitate

precipitation on the sediment of negatively charged

phosphate with positively charged complexed metals(Fe, Al, La) acting as reactive entities. These P-nutri-

ent-reducing compounds have found wide application

in reduction of eutrophication (re-oligotrophicationprogrammes) and are discussed in greater detail

elsewhere in this special issue (Douglas et al. 2016).

Calibrated minimal dosing and awareness of thechemical (pH, redox) lability of the metal-binding

substances being used will contribute to improved

appreciation of sustainability issues (Spears et al.2013). Hence, proper control of the pH and redox

conditions in all compartments of a lake is required,

also considering differences between seasons inapplications of metal-based general algistatic

compounds.

So elegant, and so little understood is the applica-tion of barley (or rice) straw. Not only uncertainty

about its effectiveness and the time span needed for

actual effects are noticeable problems, but also astrong increase in organic matter that will raise the

biological oxygen demand, makes it desirable that the

really active compound(s) will be identified, such thatextracts with these compounds can be used instead of

the raw bulk material. However, costs involved in such

a strategy are far from using cheap waste materials asalgicide directly.

HP can be a selective cyanocide as well as a more

general algicide, the difference depends on the dosingconcentration. For a general algicidal function, a 5 or

even 10 times higher concentration is needed than for a

cyanocidal application, and use of such a higherconcentration also requires special permission for

lawful application, see Burson et al. (2014) describing

a successful termination of a harmful dinoflagellatebloom. This application, however, differs from the

mild cyanocidal approach in damaging a wider range

of life in the treated water body.A final word on recommended or rather to be

discontinued usage of compounds should includeconsiderations on price, sustainability and ecosafety

of particular methods. Table 1 advises on choices that

can be made. Estimates of the amount of algicidalsubstance needed can be made from the recommended

concentrations for established applications that have

been mentioned in the main text and the adheredreferences, plus the water volume content of the lake

concerned, using the approximate product pricesindicated.

A very important issue is the duration for a

treatment to be completed including the aftermath ofresults to become apparent and the time it takes for

side effects to cease, and most obviously how long the

results of an intervention will last. The shorter theterm, the more it loads on costs and disobeys

sustainability principles. The column with applicable

dose indications therefore shows the approximateapplication frequency in different categories in

Table 1. This evaluation has been based on conclu-

sions from literature reading and interpretation of theworking mechanism. Lack of data on repeated indi-

vidual treatment plans prohibit arriving at strong

recommendations, and in many cases the establishedcriteria are therefore based on an educated guess.

As may hold for all cyanocidal compounds, lysis of

cells raises questions about the release of cyanotoxinsinto the water. For example, the use of paraquat

(1 mM) resulted in a 90 % increase in detectable tox-

ins (Ross et al. 2006). This is a potential generaldrawback of cyanocide application. A direct compar-

ison of the MC-LR release potential of copper and

other algicides like HP, diuron and ethyl 2-methy-lacetoacetate (EMA) for the four algicides showed the

order CuSO4[H2O2[ diuron[EMA (Zhou et al.

2013). However, it must be mentioned that concernsabout toxin release associated with algicide applica-

tion were based on laboratory studies using culture

collection strains that may lack the cyanotoxindegrading environmental biotome (Zhou et al. 2013;

Lurling et al. 2014).

The pertinent nature of cyanotoxin loss can bestudied easily by estimation of the actual dynamics of

the toxin content in the water after application and the

time it takes for self-contained clearance of theproblems. An early example of the fate of MC is

presented in a study on treatment effects with copper

sulphate where microcystin appeared to remain pre-sent at first, but gradually disappeared to low levels

8 days after the treatment (Jones and Orr 1994).Different cyanocides may render different results in

different environments, which may also relate to the

degree of lost or retained post-treatment microbialbiodegradation capacity after application of a cyano-

cide that may affect a wider range of prokaryotes. As

different from the rather slow microcystin disappear-ance after copper sulphate application as reported by

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123

Jones and Orr (1994), the actual disappearance wasfaster in the case of HP application where the

degradation of MC took place fairly rapidly in

2–3 days (Matthijs et al. 2012, also see ‘‘Hydrogenperoxide’’ section).

It is recommended that for all new cyanocidal

compounds, kinetic measurement of the post-treat-ment prevalence in the water of important cyanotoxins

should be included in all studies on applications of

cyanocides. These hold in particular true for thosecompounds that are known to be abundantly present at

levels above established safety management guideli-

nes, with MC as the key example, but also includinganatoxin, cylindrospermopsin, and nodularin.

It must be stressed that for additions of compounds

to water bodies and methods used regulations exist,that urge consideration of ecosafety and safety during

the proper application (some of the compounds in

more concentrated form are highly toxic to humans).However, quite some of those established regulations

are strikingly different between countries. An example

is the case of atrazine: use of atrazine is absolutelyforbidden in Europe, while use is tolerated by the US

EPA with strict dosage restrictions. Conversely, use of

HP for entire lake experiments has been temporarilyapproved by EUCHEM, but individual EU govern-

ments may restrict handling of the concentrated stock

by implementation of other legal safety rulings. Bynow, permission of HP application in the USA still

differs between states. Each and every application of

cyanocides needs permission in advance from legalauthorities, which ideally should interpret dynamic

advances in knowledge on cyanocides in the context of

the applicable law. Societal needs strongly underlinethe urgency of continued efforts to make the precious

freshwater stocks around the world healthier and more

readily available for the wide range of heavilydemanded ecosystem services. Besides maintenance

of natural beauty and rich biodiversity, it is essential to

sustain the current needs of mankind for reliable freshwater, now and in the future.

Concluding remarks

Next to a review of existing general algicidal methods,new treatments for directed suppression of uniquely

cyanobacteria, i.e. that functions as cyanocide, are

highlighted in this literature survey. The focus is onemerging cyanocidal methods with a sustainable

nature. We emphasize that the use of cyanocides isnot seen as a replacement of the principally needed

efforts to stop eutrophication and enhance re-olig-

otrophication at large by nutrient reduction. Themethods to reduce nutrient loading remain essential

for sustainable lake mitigation. To our opinion, new

cyanocidal methods can be used to accelerate lakerestoration, with a more balanced phytoplankton

community as a major attributed sustainability value.

Indeed, many of the cyanocidal methods can bepracticed in parallel with the reduction of nutrient

loading.

Acknowledgments This study was supported as a long-termresearch development Project No. RVO 67985939 (Institute ofBotany of the ASCR) and by the Czech Ministry of Education(LO1214).

Author’s contribution Authors DJ and BM contributed theintroduction, ‘‘Herbicides’’, ‘‘Algicidal function of copper’’,‘‘Natural compounds’’, ‘‘Isolated natural compounds, includingsynthetic homologues’’ and ‘‘Nanomaterials’’ sections; authorsHM and PV contributed ‘‘Potassium chloride’’ and ‘‘Hydrogenperoxide’’ section and the discussion. HM edited the manu-script. The authors are indebted to anonymous reviewers forhelpful comments and to special issue editor Dr. M. Bormans forsuggestions during the finalization of this manuscript. Allauthors have approved the final version. Authors would like toacknowledge European Cooperation in Science and TechnologyCOST action ES1105 CYANOCOST ‘‘Cyanobacterial bloomsand toxins in water resources: occurrence, impacts andmanagement’’.

Open Access This article is distributed under the terms of theCreative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unre-stricted use, distribution, and reproduction in any medium,provided you give appropriate credit to the originalauthor(s) and the source, provide a link to the Creative Com-mons license, and indicate if changes were made.

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